Skip to main content

Advertisement

SpringerLink
Log in

Regulation of allergy and autoimmunity in helminth infection

  • Published:
Clinical Reviews in Allergy & Immunology Aims and scope Submit manuscript

Abstract

Parasitic infections are a major theme in the “hygiene hypothesis”, as allergies and autoimmune diseases are less prevalent in countries with higher burdens of helminths and other parasitic organisms. Helminths”—the grouping of multicellular worm parasistes including nematodes, cestodes and trematodes—tend to establish long-liver, chronic infections indicating successful down-modulation of the host immune system. In this review, we describe the intricate immunology of host-helminth interactions and how parasites manipulate immune responses to enhance their survival. In so doing, they often minimise immunopathology and, it is suggested, reduce host susceptibility to, and severity of allergic and autoimmune diseases. Studies on helminth-infected communities and individuals support the hypothesis that an immuno-regulatory network promoted by parasites extends its influence to limiting allergies. Experimental models are now probing more deeply into the area of immune modulation by helminths, and we discuss the likely mechanisms by which helminths could be establishing a strongly regulatory environment. Understanding and harnessing the modulatory capacity of helminths may uncover novel therapeutic interventions, mimicking and exploiting their evolution for our benefit. Parasitic infections are a major theme in the—“hygiene hypothesis”, as allergies and autoimmune diseases are less prevalent in countries with higher burdens of helminths and other parasitic organisms. Helminths”—the grouping of multicellular worm parasistes including nematodes, cestodes and trematodes—tend to establish long-lived, chronic infections indicating successful down-modulation of the host immune system. In this review, we describe the intricate immunology of host-helminth interactions and how parasites manipulate immune responses to enhance their survival. In so doing, they often minimise immunopathology and, it is suggested, reduce host susceptibility to, and severity of allergic and autoimmune diseases. Studies on helminth-infected communities and individuals support the hypothesis that an immuno-regulatory network promoted by parasites extends its influence to limiting allergies. Experimental models are now probing more deeply into the area of immune modulation by helminths, and we discuss the likely mechanisms by which helminths could be establishing a strongly regulatory environment. Understanding and harnessing the modulatory capacity of helminths may uncover novel therapeutic interventions, mimicking and exploiting their evolution for our benefit.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Sher, A.F. and Coffman, R.L. (1992), Ann Rev. Immunol. 10, 385–409.

    Article  CAS  Google Scholar 

  2. Maizels, R.M., Bundy, D.A.P., Selkirk, M.E., et al. (1993), Nature 365, 797–805.

    Article  PubMed  CAS  Google Scholar 

  3. Pearce, E.J. and MacDonald, A.S. (2002), Nature Rev. Immunol. 2, 499–511.

    Article  CAS  Google Scholar 

  4. Satoguina, J., Mempel, M., Larbi, J., et al. (2002), Microbes Infect. 4, 1291–1300.

    Article  PubMed  CAS  Google Scholar 

  5. van der Kleij, D., Latz, E., Brouwers, J.F.H.M., et al. (2002), J. Biol. Chem. 277, 48,122–48,129.

    Article  Google Scholar 

  6. Maizels, R.M. and Yazdanbakhsh, M. (2003), Nature Rev. Immunol. 3, 733–743.

    Article  CAS  Google Scholar 

  7. Urban, J.F., Madden, K.B., Sveti’c, A., et al. (1992), Immunol. Rev. 127, 205–220.

    Article  PubMed  CAS  Google Scholar 

  8. Else, K.J., Finkelman, F.D., Maliszewski, C.R., and Grencis, R.K. (1994), J. Exp. Med. 179, 347–351.

    Article  PubMed  CAS  Google Scholar 

  9. Al-Qaoud, K.M., Pearlman, E., Hartung, T., et al. (1999), Int. Immunol. 12, 899–908.

    Article  Google Scholar 

  10. Ben-Smith, A., Lammas, D.A. and Behnke, J.M. (2003), J. Helminthol. 77, 133–146.

    Article  PubMed  CAS  Google Scholar 

  11. Pearce, E.J., Vasconcelos, J.P., Brunet, L.R., and Sabin, E.A. (1996), Exp. Parasitol. 84, 295–299.

    Article  PubMed  CAS  Google Scholar 

  12. Hoffmann, K.F., Cheever, A.W. and Wynn, T.A. (2000), J. Immunol. 164, 6406–6416.

    PubMed  CAS  Google Scholar 

  13. Mannino, D.M., Homa, D.M., Pertowski, C.A., et al. (1998), MMWR CPC Surveill. Summ. 47, 1–27.

    CAS  Google Scholar 

  14. ISAAC (1998), Lancet 351, 1225–1232.

    Article  Google Scholar 

  15. Woolcock, A.J. and Peat, J.K. (1997), Ciba Found. Symp. 206, 122–134.

    PubMed  CAS  Google Scholar 

  16. Woolcock, A.J., Peat, J.K., and Trevillion, L.M. (1995), Allergy 50, 935–940.

    PubMed  CAS  Google Scholar 

  17. Sears, M.R. (1997), Lancet 350, 1015–1020.

    Article  PubMed  CAS  Google Scholar 

  18. Hopkin, J.M. (1997), Curr. Opin. Immunol. 9, 788–792.

    Article  PubMed  CAS  Google Scholar 

  19. Shirakawa, T., Enomoto, T., Shimazu, S., and Hopkin, J.M.S. (1997), Science 275, 77–79.

    Article  PubMed  CAS  Google Scholar 

  20. Matricardi, P.M. and Bonini, S.S. (2000), Clin. Exp. Allergy 30, 1506–1510.

    Article  PubMed  CAS  Google Scholar 

  21. Matricardi, P.M. and Bonini, S.S. (2000), Respir. Res. 1, 129–132.

    Article  PubMed  CAS  Google Scholar 

  22. Strachan, D.P. (1989), Br. Med. J. 299, 1259–1260.

    CAS  Google Scholar 

  23. Stene, L.C. and Nafstad, P. (2001), Lancet 357, 607–608.

    Article  PubMed  CAS  Google Scholar 

  24. Bach, J.F. (2002), N. Engl. J. Med. 347, 911–920.

    Article  PubMed  Google Scholar 

  25. Kero, J., Gissler, M., Hemminki, E. and Isolauri, E.S. (2001), J. Allergy Clin. Immunol. 108, 781–783.

    Article  PubMed  CAS  Google Scholar 

  26. Simpson, C.R., Anderson, W.J., Helms, P.J., et al. (2002), Clin. Exp. Allergy 32, 37–42.

    Article  PubMed  CAS  Google Scholar 

  27. Mao, X.-Q., Sun, D.-J., Miyoshi, A., et al. (2000), Parasitol. Today 16, 186–188.

    Article  PubMed  CAS  Google Scholar 

  28. Wills-Karp, M., Santeliz, J. and Karp, C.L. (2001), Nat. Rev. Immunol. 1, 69–75.

    Article  PubMed  CAS  Google Scholar 

  29. Yazdanbakhsh, M., van den Biggelaar, A., and Maizels, R.M. (2001), Trends Immunol. 22, 372–377.

    Article  PubMed  CAS  Google Scholar 

  30. Gale, E.A.M. (2002), Diabetologia 45, 588–594.

    Article  PubMed  CAS  Google Scholar 

  31. Umetsu, D.T., McIntire, J.J., Akbari, O., et al. (2002), Nat. Immunol 3, 715–720.

    Article  PubMed  CAS  Google Scholar 

  32. Yazdanbakhsh, M., Kremsner, P.G., and van Ree, R.S. (2002), Science 296, 490–494.

    Article  PubMed  CAS  Google Scholar 

  33. Leynaert, B., Neukirch, C., Jarvis, D., et al. (2001), Am. J. Respir. Crit. Care Med. 164, 1829–1834.

    PubMed  CAS  Google Scholar 

  34. von Mutius, E.S. (2001), Am. J. Respir. Crit. Care Med. 164, 1106–1107.

    Google Scholar 

  35. Yemaneberhan, H., Bekele, Z., Venn, A., et al. (1997), Lancet 350, 85–90.

    Article  PubMed  CAS  Google Scholar 

  36. Kramer, U., Heinrich, J., Wjst, M., and Wichmann, H.E. (1999), Lancet 353, 450–454.

    Article  PubMed  CAS  Google Scholar 

  37. McKinney, P.A., Okasha, M., Parslow, R.C., et al. (2000), Diabet. Med. 17, 236–242.

    Article  PubMed  CAS  Google Scholar 

  38. van den Biggelaar, A., Ree, R.V., Roderigues, L.C., et al. (2000), Lancet 356, 1723–1727.

    Article  PubMed  Google Scholar 

  39. Karp, C.L., Wysocka, M., Wahl, L.M., et al. (1996), Science 273, 228–231.

    Article  PubMed  CAS  Google Scholar 

  40. Erb, K.J., Holloway, J.W., Sobeck, A., et al. (1998), J. Exp. Med. 187, 561–569.

    Article  PubMed  CAS  Google Scholar 

  41. Sternberg, J.M. and Mabbott, N.A. (1996), Eur. J. Immunol. 26, 539–543.

    Article  PubMed  CAS  Google Scholar 

  42. Murray, M.J., Murray, A.B., Murray, M.B., and Murray, C.J. (1977), Am. J. Clin. Nutr. 30, 2117–2121.

    PubMed  CAS  Google Scholar 

  43. Murray, J., Murray, A., Murray, M., and Murray, C. (1978), Am. J. Clin. Nutr. 31, 1363–1366.

    PubMed  CAS  Google Scholar 

  44. Nacher, M., Gay, F., Singhasivanon, P., et al. (2000), Parasite Immunol. 22, 107–113.

    Article  PubMed  CAS  Google Scholar 

  45. Nacher, M., Singhasivanon, P., Silachamroon, U., et al. (2001), Am. J. Trop. Med. Hyg. 65, 834–836.

    PubMed  CAS  Google Scholar 

  46. Sabin, E.A., Araujo, M.I., Carvalho, E.M., and Pearce, E.J. (1996), J. Infect. Dis. 173, 269–272.

    PubMed  CAS  Google Scholar 

  47. Cooper, P.J., Espinel, I., Paredes, W., et al. (1998), J. Infect. Dis. 178, 1133–1138.

    PubMed  CAS  Google Scholar 

  48. Borkow, G., Weisman, Z., Leng, Q., et al. (2001), Scand. J. Infect. Dis. 33, 568–571.

    Article  PubMed  CAS  Google Scholar 

  49. Kullberg, M.C., Pearce, E.J., Hieny, S.E., et al. (1992), J. Immunol. 148, 3264–3270.

    PubMed  CAS  Google Scholar 

  50. Actor, J.K., Shirai, M., Kullberg, M.C., et al. (1993), Proc. Natl. Acad. Sci. USA 90, 948–952.

    Article  PubMed  CAS  Google Scholar 

  51. Ledingham, D.L., McAlister, V.C., Ehigiator, H.N., et al. (1996), Transplantation 61, 184–188.

    Article  PubMed  CAS  Google Scholar 

  52. Liu, Z., Liu, Q., Pesce, J., et al. (2002), J. Immunol. 169, 6959–6968.

    PubMed  CAS  Google Scholar 

  53. Röcken, M., Urban, J.F., and Shevach, E.M. (1992), Nature 359, 79–82.

    Article  PubMed  Google Scholar 

  54. Ali, N.M. and Behnke, J.M. (1984), Parasitology 88, 153–162.

    PubMed  Google Scholar 

  55. Holland, M.J., Harcus, Y.M., Riches, P.L., and Maizels, R.M. (2000), Eur. J. Immunol. 30, 1977–1987.

    Article  PubMed  CAS  Google Scholar 

  56. Goodridge, H.S., Wilson, E.H., Harnett, W., et al. (2001), J. Immunol. 167, 940–945.

    PubMed  CAS  Google Scholar 

  57. Paterson, J.C., Garside, P., Kennedy, M.W., and Lawrence, C.E. (2002), Infect. Immun. 70, 6058–6067.

    Article  PubMed  CAS  Google Scholar 

  58. Boitelle, A., Scales, H.E., Di Lorenzo, C., et al. (2003), J. Immunol. 171, 447–454.

    PubMed  CAS  Google Scholar 

  59. van den Biggelaar, A.H., Lopuhaa, C., van Ree, R., et al. (2001), Int. Arch. Allergy Immunol. 126, 231–238.

    Article  PubMed  Google Scholar 

  60. Selassie, F.G., Stevens, R.H., Cullinan, P., et al. (2000), Clin. Exp. Allergy 30, 356–358.

    Article  PubMed  CAS  Google Scholar 

  61. Araujo, M.I., Lopes, A.A., Medeiros, M., et al. (2000), Int. Arch. Allergy Immunol. 123, 145–148.

    Article  PubMed  CAS  Google Scholar 

  62. Lynch, N.R., Hagel, I., Perez, M., et al. (1993), J. Allerg. Clin. Immunol. 92, 404–411.

    Article  CAS  Google Scholar 

  63. Nyan, O.A., Walraven, G.E.L., Banya, W.A.S., et al. (2001), Clin. Exp. Allergy 31, 1672–1678.

    Article  PubMed  CAS  Google Scholar 

  64. Scrivener, S., Yemaneberhan, H., Zebenigus, M., et al. (2001), Lancet 358, 1493–1499.

    Article  PubMed  CAS  Google Scholar 

  65. Lynch, N.R., Palenque, M., Hagel, I., and Di Prisco, M.C. (1997), Am. J. Resp. Crit. Care Med. 156, 50–54.

    PubMed  CAS  Google Scholar 

  66. Hagel, I., Lynch, N.R., DiPrisco, M.C., et al. (1993), Int. Arch. Allergy Immunol. 101, 209–214.

    Article  PubMed  CAS  Google Scholar 

  67. Cooper, P.J. (2002), Clin. Exp. Immunol. 128, 398–404.

    Article  PubMed  CAS  Google Scholar 

  68. Wang, C.C. and Rook, G.A.W. (1998), Immunology 93, 307–313.

    Article  PubMed  CAS  Google Scholar 

  69. Yang, X., Wang, S., Fan, Y., and Zhu, L. (1999), Immunology 98, 329–337.

    Article  PubMed  CAS  Google Scholar 

  70. Hopfenspirger, M.T. and Agrawal, D.K. (2002), J. Immunol. 168, 2516–2522.

    PubMed  CAS  Google Scholar 

  71. Zuany-Amorim, C., Manlius, C., Trifilieff, A., et al. (2002), J. Immunol. 169, 1492–1499.

    PubMed  CAS  Google Scholar 

  72. Zuany-Amorim, C., Sawicka, E., Manlius, C., et al. (2002), Nature Med. 8, 625–629.

    Article  PubMed  CAS  Google Scholar 

  73. Wang, C.C., Nolan, T.J., Schad, G.A. and Abraham, D. (2001), Clin. Exp. Allergy 31, 495–503.

    Article  PubMed  CAS  Google Scholar 

  74. Bashir, M.E., Andersen, P., Fuss, I.J., et al. (2002), J. Immunol. 169, 3284–3292.

    PubMed  CAS  Google Scholar 

  75. Lima, C., Perini, A., Garcia, M.L.B., et al. (2002), Clin. Exp. Allergy 32, 1659–1666.

    Article  PubMed  CAS  Google Scholar 

  76. Silveira, M.R., Nunes, K.P., Cara, D.C., et al. (2002), Infect. Immun. 70, 6263–6272.

    Article  PubMed  CAS  Google Scholar 

  77. Negrao-Correa, D., Silveira, M.R., Borges, C.M., et al. (2003), Infect. Immun. 71, 2607–2614.

    Article  PubMed  CAS  Google Scholar 

  78. Anonymous (2000), Lancet 355, 873–876.

    Article  Google Scholar 

  79. Rosati, G., Aiello, I., Mannu, L., et al. (1988), Neurology 38, 384–388.

    PubMed  CAS  Google Scholar 

  80. Farrokhyar, F., Swarbrick, E.T., and Irvine, E.J. (2001), Scand. J. Gastroenterol. 36, 2–15.

    Article  PubMed  CAS  Google Scholar 

  81. Mandrell, R.E., McLaughlin, R., Aba Kwaik, Y., et al. (1992), Infect. Immun. 60, 1322–1328.

    PubMed  CAS  Google Scholar 

  82. Harvey, H.A., Swords, W.E., and Apicella, M.A. (2001), J. Autoimmun. 16, 257–262.

    Article  PubMed  CAS  Google Scholar 

  83. Moran, A.P. and Prendergast, M.M. (2001), J. Autoimmun. 16, 241–256.

    Article  PubMed  CAS  Google Scholar 

  84. Andersen, E., Isager, H., and Hyllested, K. (1981), Acta Neurol. Scand. 63, 131–135.

    Article  PubMed  CAS  Google Scholar 

  85. Sewell, D.L., Reinke, E.K., Hogan, L.H., et al. (2002), Immunol. Lett. 82, 101–110.

    Article  PubMed  CAS  Google Scholar 

  86. Sewell, D., Qing, Z., Reinke, E., et al. (2003), Int. Immunol. 15, 59–69.

    Article  PubMed  CAS  Google Scholar 

  87. Cooke, A., Tonks, P., Jones, F.M., et al. (1999), Parasite Immunol. 21, 169–176.

    Article  PubMed  CAS  Google Scholar 

  88. Zaccone, P., Fehervari, Z., Jones, F.M., et al. (2003), Eur. J. Immunol. 33, 1439–1449.

    Article  PubMed  CAS  Google Scholar 

  89. Elliott, D.E., Li, J., Blum, A., et al. (2003), Am. J. Physiol. Gastrointest. Liver Physiol. 284, G385-G391.

    PubMed  CAS  Google Scholar 

  90. Khan, W.I., Blennerhasset, P.A., Varghese, A.K., et al. (2002), Infect. Immun. 70, 5931–5937.

    Article  PubMed  CAS  Google Scholar 

  91. Fox, J.G., Beck, P., Dangler, C.A., et al. (2000), Nature Med. 6, 536–542.

    Article  PubMed  CAS  Google Scholar 

  92. Berg, D.J., Davidson, N., Kuhn, R., et al. (1996), J. Clin. Invest. 98, 1010–1020.

    PubMed  CAS  Google Scholar 

  93. Elliott, D.E., Urban, J.F. Jr., Argo, C.K., and Weinstock, J.V. (2000), FASEB J. 14, 1848–1855.

    Article  PubMed  CAS  Google Scholar 

  94. Imai, S., Tezuka, H., and Fujita, K. (2001), Biochem. Biophys. Res. Commun. 286, 1051–1058.

    Article  PubMed  CAS  Google Scholar 

  95. Kennedy, M.W. (2000), Parasitol. Today 16, 373–380.

    Article  PubMed  CAS  Google Scholar 

  96. Barthlott, T., Kassiotis, G., and Stockinger, B. (2003), J. Exp. Med. 197, 451–460.

    Article  PubMed  CAS  Google Scholar 

  97. Stockinger, B., Barthlott, T., and Kassiotis, G. (2001), Nat. Immunol. 2, 757–758.

    Article  PubMed  CAS  Google Scholar 

  98. Lynch, N.R., Goldblatt, J., and Le Souef, P.N.S. (1999), Thorax 54, 659–660.

    PubMed  CAS  Google Scholar 

  99. Kawakami, T. and Galli, S.J. (2002), Nat. Rev. Immunol. 2, 773–786.

    Article  PubMed  CAS  Google Scholar 

  100. Mehlhop, P.D., van de Rijn, M., Goldberg, A.B., et al. (1997), Proc. Natl. Acad. Sci. USA 94, 1344–1349.

    Article  PubMed  CAS  Google Scholar 

  101. Williams, C.M. and Galli, S.J. (2000), J. Allergy Clin. Immunol. 105, 847–859.

    Article  PubMed  CAS  Google Scholar 

  102. Williams, C.M. and Galli, S.J. (2000), J. Exp. Med. 192, 455–462.

    Article  PubMed  CAS  Google Scholar 

  103. Dehlawi, M.S., Wakelin, D., and Behnke, J.M. (1987), Parasite Immunol. 9, 187–194.

    PubMed  CAS  Google Scholar 

  104. Yamaguchi, M., Sayama, K., Yano, K., et al. (1999), J. Immunol. 162, 5455–5465.

    PubMed  CAS  Google Scholar 

  105. McDermott, J.R., Bartram, R.E., Knight, P.A., et al. (2003), Proc. Natl. Acad. Sci. USA 100, 7761–7766.

    Article  PubMed  CAS  Google Scholar 

  106. Knight, P.A., Wright, S.H., Lawrence, C.E., et al. (2000), J. Exp. Med. 192, 1849–1856.

    Article  PubMed  CAS  Google Scholar 

  107. Robbie-Ryan, M. and Brown, M. (2002), Curr. Opin. Immunol. 14, 728–733.

    Article  PubMed  CAS  Google Scholar 

  108. Royer, B., Varadaradjalou, S., Saas, P., et al. (2001), Clin. Exp. Allergy 31, 694–704.

    Article  PubMed  CAS  Google Scholar 

  109. Hamelmann, E. and Gelfand, E.W. (2001), Immunol. Rev. 179, 182–191.

    Article  PubMed  CAS  Google Scholar 

  110. Hamelmann, E., Cieslewicz, G., Schwarze, J., et al. (1999), Am. J. Respir. Crit. Care Med. 160, 934–941.

    PubMed  CAS  Google Scholar 

  111. Brown, T.R. (1898), J. Exp. Med. 3, 315–347.

    Article  PubMed  CAS  Google Scholar 

  112. Meeusen, E.N.T. and Balic, A. (2000), Parasitol. Today 16, 95–101.

    Article  PubMed  CAS  Google Scholar 

  113. Hall, L.R., Lass, J.H., Diaconu, E., et al. (1999), J. Immunol. 163, 4970–4975.

    PubMed  CAS  Google Scholar 

  114. Culley, F.J., Brown, A., Conroy, D.M., et al. (2000), J. Immunol. 165, 6447–6453.

    PubMed  CAS  Google Scholar 

  115. Angeli, V., Faveeuw, C., Delerive, P., et al. (2001), Eur. J. Immunol. 31, 2751–2761.

    Article  PubMed  CAS  Google Scholar 

  116. Romagnani, S. (1994), Annu. Rev. Immunol. 12, 227–257.

    Article  PubMed  CAS  Google Scholar 

  117. Bilenki, L., Wang, S., Fan, Y., et al. (2002), Clin. Immunol. 102, 28–36.

    Article  PubMed  CAS  Google Scholar 

  118. Tsitoura, D.C., Blumenthal, R.L., Berry, G., et al. (2000), J. Allergy Clin. Immunol. 106, 239–246.

    Article  PubMed  CAS  Google Scholar 

  119. Hansen, G., Berry, G., DeKruyff, R.H., and Umetsu, D.T.S. (1999), J. Clin. Invest. 103, 175–183.

    PubMed  CAS  Google Scholar 

  120. Allen, J.E. and Maizels, R.M. (1997), Immunol. Today 18, 387–392.

    Article  PubMed  CAS  Google Scholar 

  121. Platts-Mills, T., Vaughan, J., Squillace, S., et al. (2001), Lancet 357, 752–756.

    Article  PubMed  CAS  Google Scholar 

  122. Platts-Mills, T.A., Vaughan, J.W., Blumenthal, K., et al. (2001), Int. Arch. Allergy Immunol. 124, 126–129.

    Article  PubMed  CAS  Google Scholar 

  123. Hussain, R., Poindexter, R.W., and Ottesen, E.A. (1992), J. Immunol. 148, 2731–2737.

    PubMed  CAS  Google Scholar 

  124. Kurniawan, A., Yazdanbakhsh, M., van Ree, R., et al. (1993), J. Immunol. 150, 3941–3950.

    PubMed  CAS  Google Scholar 

  125. Jeannin, P., Lecoanet, S., Delneste, Y., et al. (1998), J. Immunol. 160, 3555–3561.

    PubMed  CAS  Google Scholar 

  126. Cooper, P.J., Chico, M.E., Rodrigues, L.C., et al. (2003), J. Allergy Clin. Immunol. 111, 995–1000.

    Article  PubMed  Google Scholar 

  127. Lukacs, N.W. (2001), Nat. Rev. Immunol. 1, 108–116.

    Article  PubMed  CAS  Google Scholar 

  128. Nakae, S., Komiyama, Y., Yokoyama, H., et al. (2003), Int. Immunol 15, 483–490.

    Article  PubMed  CAS  Google Scholar 

  129. Schopf, L.R., Hoffmann, K.F., Cheever, A.W., et al. (2002), J. Immunol. 168, 2383–2392.

    PubMed  CAS  Google Scholar 

  130. Wills-Karp, M. and Chiaramonte, M. (2003), Curr. Opin. Pulm. Med. 9, 21–27.

    Article  PubMed  CAS  Google Scholar 

  131. Wynn, T.A. (2003), Annu. Rev. Immunol. 21, 425–456.

    Article  PubMed  CAS  Google Scholar 

  132. Herrick, C.A., Xu, L., McKenzie, A.N., et al. (2003), J. Immunol. 170, 2488–2495.

    PubMed  CAS  Google Scholar 

  133. Chiaramonte, M.G., Donaldson, D.D., Cheever, A.W., and Wynn, T.A. (1999), J. Clin. Invest. 104, 777–785.

    PubMed  CAS  Google Scholar 

  134. Walter, D.M., McIntire, J.J., Berry, G., et al. (2001), J. Immunol. 167, 4668–4675.

    PubMed  CAS  Google Scholar 

  135. Grünig, G., Warnock, M., Wakil, A.E., et al. (1998), Science 282, 2261–2263.

    Article  PubMed  Google Scholar 

  136. Wills-Karp, M., Luyimbazi, J., Xu, X., et al. (1998), Science 282, 2258–2261.

    Article  PubMed  CAS  Google Scholar 

  137. Chiaramonte, M.G., Mentink-Kane, M., Jacobson, B.A., et al. (2003), J. Exp. Med. 197, 687–701.

    Article  PubMed  CAS  Google Scholar 

  138. Akbari, O., Stock, P., DeKruyff, R.H., and Umetsu, D.T. (2003), Int. Arch. Allergy Immunol. 130, 108–118.

    Article  PubMed  Google Scholar 

  139. Herrick, C.A. and Bottomly, K. (2003), Nat. Rev. Immunol. 3, 405–412.

    Article  PubMed  CAS  Google Scholar 

  140. Groux, H., O’Garra, A., Bigler, M., et al. (1997), Nature 389, 737–742.

    Article  PubMed  CAS  Google Scholar 

  141. Sakaguchi, S. (2000), Cell 101, 455–458.

    Article  PubMed  CAS  Google Scholar 

  142. Maloy, K.J. and Powrie, F. (2001), Nat. Immunol. 2, 816–822.

    Article  PubMed  CAS  Google Scholar 

  143. Sakaguchi, S., Sakaguchi, N., Shimizu, J., et al. (2001), Immunol. Rev. 182, 18–32.

    Article  PubMed  CAS  Google Scholar 

  144. Apostolou, I., Sarukhan, A., Klein, L., and von Boehmer, H. (2002), Nat. Immunol. 3, 756–763.

    PubMed  CAS  Google Scholar 

  145. Belkaid, Y., Piccirillo, C.A., Mendez, S., et al. (2002), Nature 420, 502–507.

    Article  PubMed  CAS  Google Scholar 

  146. McGuirk, P., McCann, C., and Mills, K.H. (2002), J. Exp. Med. 195, 221–231.

    Article  PubMed  CAS  Google Scholar 

  147. Fontenot, J.D., Gavin, M.A., and Rudensky, A.Y. (2003), Nat. Immunol. 4, 330–336.

    Article  PubMed  CAS  Google Scholar 

  148. Khattri, R., Cox, T., Yasayko, S.A., and Ramsdell, F. (2003), Nat. Immunol. 4, 337–342.

    Article  PubMed  CAS  Google Scholar 

  149. Yazdanbakhsh, M., Paxton, W.A., Kruize, Y.C., et al. (1993), J. Infect. Dis. 167, 925–931.

    PubMed  CAS  Google Scholar 

  150. Sartono, E., Kruize, Y.C., Partono, F., et al (1995), Parasite Immunol. 17, 587–594.

    PubMed  CAS  Google Scholar 

  151. Mahanty, S., Mollis, S.N., Ravichandran, M., et al. (1996), J. Infect. Dis. 173, 769–773.

    PubMed  CAS  Google Scholar 

  152. Schonemeyer, A., Lucius, R., Sonnenburg, B., et al. (2001), J. Immunol. 167, 3207–3215.

    PubMed  CAS  Google Scholar 

  153. Doetze, A., Satoguina, J., Burchard, G., et al. (2000), Int. Immunol. 12, 623–630.

    Article  PubMed  CAS  Google Scholar 

  154. Hadeiba, H. and Locksley, R.M. (2003), J. Immunol. 170, 5502–5510.

    PubMed  CAS  Google Scholar 

  155. Akbari, O., Freeman, G.J., Meyer, E.H., et al. (2002), Nature Med. 8, 1024–1032.

    Article  PubMed  CAS  Google Scholar 

  156. Jutel, M., Akdis, M., Budak, F., et al. (2003), Eur. J. Immunol. 33, 1205–1214.

    Article  PubMed  CAS  Google Scholar 

  157. Oh, J.W., Seroogy, C.M., Meyer, E.H., et al. (2002), J. Allergy Clin. Immunol. 110, 460–468.

    Article  PubMed  CAS  Google Scholar 

  158. Hansen, G., McIntire, J.J., Yeung, V.P., et al. (2000), J. Clin. Invest. 105, 61–70.

    Article  PubMed  CAS  Google Scholar 

  159. Kohm, A.P., Carpentier, P.A., Anger, H.A., and Miller, S.D. (2002), J. Immunol. 169, 4712–4716.

    PubMed  CAS  Google Scholar 

  160. Holt, P.G. (1996), J. Exp. Med. 183, 1297–1301.

    Article  PubMed  CAS  Google Scholar 

  161. Farooqi, I.S. and Hopkin, J.M. (1998), Thorax 53, 927–932.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK

    Mark S. Wilson & Rick M. Maizels

Authors
  1. Mark S. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rick M. Maizels
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rick M. Maizels.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wilson, M.S., Maizels, R.M. Regulation of allergy and autoimmunity in helminth infection. Clinic Rev Allerg Immunol 26, 35–50 (2004). https://doi.org/10.1385/CRIAI:26:1:35

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/CRIAI:26:1:35

Index Entries

Search

Navigation